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Abstract

Long distance cell-to-cell communication is critical for the development of multicellular organisms. In this respect, plants are especially demanding as they constantly integrate environmental inputs to adjust growth processes to different conditions. One example is thickening of shoots and roots, also designated as secondary growth. Secondary growth is mediated by the vascular cambium, a stem cell-like tissue whose cell-proliferating activity is regulated over a long distance by the plant hormone auxin. How auxin signaling is integrated at the level of cambium cells and how cambium activity is coordinated with other growth processes are largely unknown. Here, we provide physiological, genetic, and pharmacological evidence that strigolactones (SLs), a group of plant hormones recently described to be involved in the repression of shoot branching, positively regulate cambial activity and that this function is conserved among species. We show that SL signaling in the vascular cambium itself is sufficient for cambium stimulation and that it interacts strongly with the auxin signaling pathway. Our results provide a model of how auxin-based long-distance signaling is translated into cambium activity and suggest that SLs act as general modulators of plant growth forms linking the control of shoot branching with the thickening of stems and roots.

Hormone-based long-distance signaling is essential for coordinating the growth and activity of different organs and tissues during the life cycle of multicellular organisms. In particular, plants are demanding in this respect because, due to their sessile and indeterminate lifestyle, their reproductive success depends on the competence to adjust their developmental programs to changing environmental conditions and requirements. Auxin is one of the best-characterized hormones involved in long-distance signaling, regulating a tremendous number of developmental processes. One of these is apical dominance, which, indeed, represents a classical example for long-distance signaling in plants (1). In this case, apex-derived auxin is transported basipetally along the main shoot and this is required for suppressing the outgrowth of axillary buds. Another process that depends on the basipetal transport of auxin is secondary growth (2). Secondary or lateral growth of growth axes is based on the activity of the vascular cambium, a meristematic tissue organized as a cylinder encompassing the center of growth axes. Cambium activity leads to the production of secondary vascular tissue, which results in an increase of shoot or root diameter. The interruptibility of the process by decapitation of the shoot tip and the subsequent reversibility by artificial auxin application is shared between apical dominance and secondary growth (1, 2). Even though both processes thus share upstream processes and, presumably, regulators, how basipetal transport of auxin is translated into two different outputs and to what degree they are interconnected is unknown.

Significant progress has been made in the understanding of the molecular control of apical dominance by the characterization of the strigolactone (SL) biosynthesis and signaling pathway. SLs, a carotenoid-derived group of molecules, show all attributes of plant hormones, meaning that they travel through the plant (3) and are effective at low concentrations (4, 5). In addition to shoot branching, SLs have been identified as germination stimulants of parasitic plants and as triggers for the establishment of interactions with mycorrhizal fungi, in which context they were originally identified (reviewed in ref. 6). The SL signaling pathway has, so far, been defined by a series of four genes for which homologs have been characterized in Arabidopsis (7–10), pea (11), petunia (12), tomato (13), and rice (14). Also in rice, two additional genes associated with the SL pathway have been recently described, indicating that the discovery of SL-related genes is not yet completed (15, 16). The identification of SL signaling in distantly related species, among them mono- and dicotyledonous species, suggests that this communication tool represents an ancient invention and that it is widely distributed within the plant kingdom.

The function of SL-related genes is characterized best in Arabidopsis where three of four MORE AXILLARY BRANCHES (MAX) proteins (MAX1, MAX3, and MAX4) have been suggested to be involved in the biosynthesis of SLs starting from carotenoids. This suggestion is based on their resemblance to carotenoid dioxygenases (MAX3 and -4) and to cytochrome P450 family members (MAX1), on corresponding biochemical activities (7–9) and on SL deficiency of knockout mutants (4, 5, 17). In contrast to max1, -3, and -4 mutants, max2 mutants are SL insensitive with regard to an effect on apical dominance (4, 5, 9), consistent with the idea that MAX2 functions as a receptor for SLs or an unknown downstream product. Moreover, its similarity to F-box leucin-rich repeat proteins and its physical interaction with compounds of Skp/Cullin/F-box (SCF) E3 ligase complexes suggests that MAX2 functions as an SL-dependent recruiting factor for proteins destined for proteasomal degradation (10).

max2 mutants (which were also isolated as ore9) (18) display various growth alterations in addition to a decrease of apical dominance, like delayed leaf senescence (18, 19), altered leaf morphology (19), and hypocotyl elongation (20). In addition, the MAX2 gene is required for karrikin-induced seed germination in postfire environments (21) and a role of the SL signaling pathway in the regulation of root system architecture was also described recently (17, 22, 23). Intriguingly, in contrast to pea and rice (4, 24), SLs are only reduced by 50% in Arabidopsis max1 and max4 mutants (17). Together, these observations suggest that the broadness of SL-dependent processes is currently underestimated.

One explanation for a broader role of the SL signaling pathway in various developmental processes is an interactive mode of action with the auxin signaling pathway. The interaction between both pathways seems to exist on several levels. On the one hand, the influence of SL signaling on auxin transport has been reported. max mutants in Arabidopsis display an enhanced expression of PIN1 and PIN3, two members of the auxin efflux transporter family and show an increase in auxin transport capacity (25–29). These observations indicate that SLs act indirectly on apical dominance by repressing auxin transport, which impedes auxin synthesized in lateral buds to be transported into the main stem (25, 29, 30). On the other hand, SL-dependent inhibition of the outgrowth of side shoots functions also in auxin-depleted plants and the application of SLs and auxin transport inhibitors, like N-1-naphthylphthalamic acid (NPA), results in different physiological responses (26). This suggests SL's function to also be downstream of auxin signaling. In fact, MAX4 and RMS1, its homolog in pea, are inducible by auxin application (7, 31), and the same holds true for RMS5, the pea homolog of MAX3 (32). Even though the significance of MAX4 inducibility has been questioned (33), these observations indicate that SL biosynthesis is stimulated by auxin.

In this study, we reveal a role of SL signaling in the regulation of secondary growth and show that the regulation of cambium activity is an SL response, which is independent from the regulation of apical dominance and conserved among species. On the basis of genetic and pharmacological data, we propose that SLs fulfill their roles directly in the cambium mainly downstream of auxin signaling.

Results

To characterize long-distance regulation of the cambium, we studied the effect of SLs on cambium activity in wild-type and max mutant Arabidopsis plants. Cambium activity was defined by the lateral extension of the tissue produced by the interfascicular cambium (IC) immediately above the uppermost rosette leaf (IC-derived tissue; ICD) and by the acropetal progression of IC initiation along the inflorescence stem (34, 35). Quantifying these parameters, we observed that the IC-based tissue production was decreased by 30% in all max mutants (Fig. 1 A–E) and that the progression of IC initiation was reduced on average by 40% (Fig. 1F). Consistent with a reduced cambium activity in SL-defective plants, qRT-PCR analyses demonstrated lower transcript levels of cambium-specific (35) and cell cycle-related (36, 37) genes in max1-1 stems in comparison with wild type (Fig. S1). Together, these observations demonstrate that plants with reduced SL signaling or biosynthesis show reduced cambium activity.

Genetic analysis of the role of SL signaling and biosynthesis in cambium regulation. (A–D) Cross-sections from immediately above the uppermost rosette leaf of wild-type (A and B) and max1-1 (C and D) stems. Note that B and D are higher magnification images for areas labeled in A and C, respectively. The extension of the IC-derived tissue (ICD) is indicated by braces (}). [Scale bar in C (100 μm) also applies to A, and scale bar in D (50 μm) also applies to B.] Asterisks indicate the position of primary vascular bundles. (E) Quantification of lateral ICD extension immediately above the uppermost rosette leaf as indicated in A and C. (F) Quantification of the longitudinal progression of IC initiation, as illustrated in D. (G) Scheme of longitudinal IC extension in the Arabidopsis stem (red) and the relative position of the treatment zone described in Fig. 2 and Fig. 4.

Local GR24 Treatments Stimulate Cambium Activity.

To test whether the reduction in cambium activity in max mutants is based on a direct regulation of the vascular cambium by SLs, we treated wild-type, max1-1, and max2-1 stems locally with the synthetic SL analog GR24. Stems were treated and analyzed in the first internode of the main inflorescence stem in a region where, without treatment, no IC is established in any of the genotypes used in this study (Fig. 1G) (34). In contrast to mock treatments, locally applied GR24 induced cell divisions in interfascicular regions of plants of all three genetic backgrounds at the treatment site (Fig. 2 A–C). The pattern of cell divisions was similar to that observed during secondary growth initiation at the base of the inflorescence stem of untreated plants (Fig. 1 A and B) (34), and the effect was dose dependent (Fig. S2A). max1-1 mutants were more sensitive than wild type and, consistent with the employment of the canonical SL signaling pathway, the effect was significantly weaker in max2-1 (Fig. 2C). Remarkably, max2-1 plants were not fully GR24 insensitive with respect to the induction of cambium-like cell divisions, which is in contrast to their insensitivity with respect to other processes (5, 23) and suggests that there are factors acting in parallel to MAX2 in this case. Collectively, these observations show that GR24 can locally stimulate cambium-like cell divisions in the Arabidopsis inflorescence stem.

GR24 treatments stimulate secondary growth in Arabidopsis inflorescence stems. (A and B) Sections from GR24- (A) and mock-treated (B) wild-type plants. Extension of tissue produced in interfascicular regions is indicated by the brace (}) in A. (C) Quantification of GR24-induced tissue production in interfascicular regions of wild-type, max1-1, and max2-1. Note that in mock-treated plants no cell divisions were observed in any of the genetic backgrounds (shown here for wild type). (D and E) PXY:CFP activity in mock- (D) and GR24-treated plants (E). Reporter gene-derived signal in the fascicular cambium is indicated by arrows in D and in interfascicular regions in E. (F and G) APL:CFP activity in mock- (F) and GR24-treated plants (G). Reporter gene-derived signal in the phloem of vascular bundles is indicated by arrows in F and in interfascicular regions in G. (H) APL:GUS activity in GR24- (Left) and mock-treated (Right) plants. (G) PXY:GUS detection in GR24- (Left) and mock-treated (Right) plants. Asterisks indicate the position of vascular bundles. [Scale bar in B (100 μm) also applies to A; scale bar in D (100 μm) also applies to E–G; scale bar in I (5 mm) also applies to H.] Note that sections in D–G were counterstained by propidium iodide (red), which highlights cell walls.

Next, we tested whether GR24-induced cell divisions represent secondary growth as observed under natural conditions by analyzing the dynamics of cambium- and phloem-specific markers in response to GR24 treatments. PHLOEM INTERCALATED WITH XYLEM (PXY, also known as TDIF RECEPTOR, TDR) is a receptor-like kinase expressed in cambium cells throughout the Arabidopsis plant body (38, 39). A reporter line expressing the cyan fluorescent protein (CFP) under the control of the PXY promoter (PXY:CFP) visualized the fascicular cambium in primary stems and, after GR24 treatments, was detected in interfascicular regions indicating GR24-induced formation of the interfascicular cambium (Fig. 2 D and E). To visualize the formation of secondary vascular tissue, we used the promoter of the APL gene encoding for a MYELOBLASTOSIS (MYB) transcription factor specifically expressed in phloem tissues (40). Initially only active in the phloem of primary bundles, an APL:CFP reporter was also active in clusters of cells in interfascicular regions after stems were treated with GR24 (Fig. 2 F and G), indicating GR24-dependent formation of secondary vascular tissue. To characterize the spatial extension of the GR24-dependent effect, we treated two reporter lines expressing the β-glucuronidase (GUS) gene under the control of the PXY and APL promoters, respectively. GR24 treatments resulted in the induction of both reporters in the treatment zone and not extending outwards by more than 0.5 cm (Fig. 2 H and I). Importantly, our treatments did not repress the outgrowth of rosette branches (Fig. S2B). Together, these results demonstrate a local induction of the cambium-specific stem cell niche and of vascular tissue formation by GR24 applications and suggest that a local increase in SL levels is capable of stimulating secondary growth in Arabidopsis inflorescence stems independently from an effect on shoot branching.

Previous reports showed that SL signaling can reduce auxin transport in the Arabidopsis stem (25–27, 29), presumably by suppressing members of the PIN family of auxin transporters (25, 28, 29). Furthermore, the analysis of auxin-sensitive reporters and measurements of auxin exported out of isolated stem fragments suggest that auxin levels are increased in max mutant backgrounds (25, 28). Because auxin is a positive key regulator of cambium activity (35, 41, 42), we thus analyzed whether SLs stimulate cambium activity indirectly by repressing auxin transport, which might result in enhanced auxin accumulation in certain cell types. Initially, we analyzed pin1-613 and pin3-5 mutants to see how changes in auxin transport capacities influence cambium activity. Both mutants were chosen because PIN1 and PIN3 are strongly expressed in stems (Fig. S2C) and, at least for pin1 mutants, it has been shown that auxin transport capacity along the stem is strongly impaired (43). Histological analysis of the acropetal progression of IC initiation and ICD extension revealed a decrease in both pin mutants (Fig. 3A and Fig. S3), implying that basipetal auxin transport along the stem is positively correlated with cambium activity and that an enhanced auxin transport rate in max mutants is not causal for decreased cambium activity.

Auxin levels and signaling are enhanced in max1 mutants. (A) In pin1-613 and pin3-5 mutants, the acropetal progression of IC initiation is diminished. Plants were analyzed when shoots were 2, 5, 15, and 30 cm tall. (B) Comparison of levels of free IAA in wild type and max1-1 at different positions along the inflorescence stem. The first elongated internode above the rosette was counted as the first internode. IN, internode. (C and D) Analysis of DR5:GUS activity in wild-type (C) and max1-1 inflorescence stems (D). Rosette leaves have been removed for clarity. (E–H) Analysis of DR5rev:GFP activity at different positions of the inflorescence stem. (E and F) DR5rev:GFP detection 1 cm above the rosette in wild type (E) and max1-1 (F). (G and H) DR5rev:GFP detection immediately above the uppermost rosette leaf of wild type (G) and max1-1 (H). [Scale bar in D (5 mm) also applies to C; scale bar in E (100 μm) also applies to F–H.]

Next, we measured the concentration of free indole-3-acetic acid (IAA) in the stems of wild-type and max1-1 mutants at different positions including the segment immediately above the uppermost rosette leaf displaying pronounced cambium activity (34). Our analyses revealed enhanced IAA concentration in max1-1 stems at all positions with an increasing difference toward the shoot base, where max1-1 contained ∼5.5 times more IAA in comparison with wild type (Fig. 3B). To determine whether enhanced IAA concentration also leads to enhanced auxin signaling, especially in segments with prominent secondary growth, we analyzed DR5:GUS reporter activity visualizing auxin signaling (44) in stems of both wild-type and max1-1 mutants. Enhanced reporter gene activity was detected in max1-1 along the whole stem including the base, where secondary growth is most prominent (34) (Fig. 3 C and D). We also analyzed the distribution of auxin signaling at tissue level resolution in wild-type and max1-1 backgrounds taking advantage of the DR5rev:GFP reporter (45). The analysis of stem cross-sections revealed a comparable pattern of reporter gene activity with more intense activity in max1-1 than in wild type. Increased reporter gene activity was observed in tissues including primary bundles along the whole stem and in interfascicular regions at the stem base where IC formation takes place (Fig. 3 E–H).

Collectively, these results show that, even though secondary growth is reduced, auxin concentration and signaling is enhanced in the vasculature of plants with reduced SL biosynthesis. This suggests that the decrease in secondary growth observed in max mutants is not a consequence of decreased auxin levels, supporting a direct role of SL signaling in the regulation of cambium activity independently or downstream of auxin accumulation.

Single Signaling Pathway for Auxin and SL in Secondary Growth Regulation.

Local treatments of stems by NPA are able to block basipetal auxin transport leading to auxin accumulation above the treatment zone and local initiation of secondary growth (36, 41, 46). We took advantage of this effect to decipher the interaction of auxin and SL signaling pathways. We speculated that if SL signaling is important for a positive effect of auxin on cambium activity, then max mutants should exhibit either no response or, at least, a weaker response than wild type. To test this hypothesis, we performed local NPA treatments of wild-type, max1-1, and max2-1 stems. We observed that interfascicular tissue production in NPA-treated max1-1 and max2-1 mutants was reduced by 75% (Fig. 4A), indicating that SL biosynthesis and signaling is important for auxin to stimulate vascular cambium activity. The fact that max mutants are not completely devoid of cambium activity might be explained by an SL-independent effect of auxin on the cambium or alternatively, by redundancy in the MAX pathway or a role of as yet unidentified factors.

Genetic interaction between axr1 and max mutants and the effect of tissue-specific SL signaling. (A) Quantification of NPA-induced tissue production in interfascicular regions of wild type, max1-1, max2-1, axr1-3, axr1-3 max1-1, and axr1-3 max2-1. (B) Quantification of GR24-induced tissue production in interfascicular regions of wild type, max1-1, max2-1, axr1-3, axr1-3 max1-1, and axr1-3 max2-1. Note that in mock-treated plants no interfascicular cell divisions were observed in any of the genetic backgrounds (shown here for wild type). (C) Quantification of lateral ICD extension immediately above the uppermost rosette leaf in wild-type, max2-1, and max2-1 plants carrying APL:MAX2, NST3:MAX2, SCR:MAX2, or WOX4:MAX2 transgenes. For each construct, two independent transgenic lines were analyzed. In all cases, n = 10.

To determine whether SL and auxin signaling might act sequentially or in parallel, we tested the genetic interaction between the axr1-3 and max mutants. axr1-3 mutants are impaired in auxin signaling (47) and we reasoned that mutant phenotypes should not be additive if both act through a common signaling pathway. Consistent with a role of AXR1 in cambium regulation, IC initiation and activity was reduced in axr1-3 mutants (Fig. S4). As expected, axr1-3 max double mutants displayed the same reduction in the NPA response as the corresponding single mutants (Fig. 4A). These findings support a sequential order of the two signaling pathways and, together with the observation of elevated auxin levels in max1-1 mutants and their reduced NPA responsiveness, suggest that SLs act downstream of auxin in a common signaling cascade. If this is the case, the axr1-3 mutation should not reduce GR24 responsiveness. Indeed, histological analyses showed that axr1-3, axr1-3 max1-1, and axr1-3 max2-1 plants displayed the same GR24-induced response as wild type, max1-1, and max2-1, respectively (Fig. 4B). Taken together, these results indicate that SLs function predominantly downstream of auxin in a signaling cascade that positively regulates secondary growth.

Tissue-Specific SL Signaling.

MAX2 activity can be found in a broad spectrum of tissues (10) and the other MAX genes can influence shoot branching over long distances (3). To dissect whether SL signaling in the vascular cambium is sufficient for stimulating cambium activity, we expressed MAX2 under the control of the (pro)cambium-specific WOX4 promoter (48) in max2-1 mutants. As controls, we also established lines expressing MAX2 in the starch sheath, phloem, and xylem, with the help of the SCR (49), APL (40), and NST3 (50) promoters, respectively. RT-PCR with primers specific for the respective constructs demonstrated that all transgenes were actively transcribed (Fig. S2D). We analyzed the lateral ICD extension at the base of the main inflorescence stem from two independent lines for each construct. This analysis demonstrated that only the lines expressing MAX2 in the vascular cambium displayed secondary growth at wild-type-like levels (Fig. 4C). Lines expressing MAX2 within the phloem or the starch sheath displayed no difference compared with max2-1, whereas only a minor increase could be observed in lines expressing MAX2 in the xylem (Fig. 4C). All in all, our results show that SL signaling within the vascular cambium is sufficient to promote cambium activity arguing that MAX2-dependent SL signaling regulates the process in a cell-autonomous manner.

SL-Dependent Cambium Regulation Is Conserved Between Species.

To elucidate whether SLs fulfill a positive role in cambium regulation in woody species displaying prominent secondary growth, we performed local GR24 treatments on stems of Eucalyptus globulus. As a result, we observed a significant increase in the production of secondary vascular tissues and in particular, the lateral extension of the cambium zone was increased (Fig. S5). To see whether the endogenous SL pathway itself is involved in cambium regulation in species other than Arabidopsis, we quantified cambium activity in the pea mutant rms1-1, impaired in the activity of the MAX4 ortholog (7, 32). Our analysis revealed a significant reduction in cambium activity in comparison with wild type (Fig. S6). Collectively, these results suggest a conserved role for SLs in the regulation of cambium activity across species, including species with prominent wood production.

Discussion

In this work, we present the role of SLs and their interaction with the auxin signaling pathway in the control of secondary growth. We report a significant reduction in cambium activity in SL-deficient mutants (Fig. 1) and show induction of secondary growth upon local treatments with the SL analog GR24 (Figs. 1 and 2). Collectively, these results demonstrate a positive role of SL signaling in the regulation of cambium activity.

Previous studies have shown that PIN protein levels and auxin transport capacity are enhanced in max1-1 mutant stems and that GR24 applications reduce PIN1 protein levels and dampen auxin transport (25, 29). It could, hence, be possible that an SL-induced change in auxin transport is the reason for an effect of SL signaling on cambium activity. However, several observations support an influence of SLs on cambium activity, which is mainly independent from regulating auxin transport. First, cambium activity is reduced in pin1 and pin3 mutants (Fig. 3), indicating that, in general, basipetal auxin transport along the stem is positively correlated with cambium activity. Second, even though cambium activity is decreased, auxin concentration and signaling is increased in the stem of max1-1 mutants. Third, genetic analyses of the interaction between SL and auxin signaling in the context of cambium regulation are in line with a requirement of SL signaling for auxin becoming fully active on cambium cells and show that SL responsiveness is not impaired in auxin signaling mutants (Fig. 4). Moreover, the axr1-3 max1-1 and axr1-3 max2-1 double mutants did not display additive phenotypes in comparison with single mutants arguing for a linear relationship of both signaling pathways.

Recently, it was shown that auxin induces the expression of the SL biosynthesis genes MAX3 and MAX4 in the stem of Arabidopsis in an AXR1-dependent manner (51). In agreement with that observation, we propose that the reduced responsiveness of axr1-3 and max1-1 toward NPA is, at least partly, due to a reduced SL biosynthesis. In the case of axr1-3, this model would imply that exogenous SL applications can bypass auxin signaling in the induction of secondary growth. In the case of max1-1, GR24 treatments would stimulate cambium activity largely independently from an effect on the auxin signaling pathway. Together with the idea that there is SL production in the shoot (3) and the observation that the expression of MAX2 in the cambium is sufficient to restore wild-type–like levels of cambium activity (Fig. 4), these results argue for an important role of auxin-dependent stimulation of SL biosynthesis in the cambium for secondary growth. As the evidence presented in this study is rather indirect, we want to point out, however, that our interpretation does not exclude the possibility that SLs influence cambium activity also by regulating auxin transport.

Importantly, the reduction of cambium activity in the pea mutant rms1-1 (impaired in SL biosynthesis) as well as the positive effect of GR24 treatments on the production of secondary vascular tissue in Eucalyptus, demonstrate that the role of SL in cambium activity is conserved among species and that it represents a common signaling mechanism for coordinating growth of different plant organs.

Conclusions

The converse effects of SLs on branching and secondary growth suggest a central role for SL in regulating plant architecture. Shoot branching and secondary growth are both influenced by environmental stimuli such as shading, temperature, or day length (52–55). On the basis of our finding that SLs are involved in the regulation of both these processes, we hypothesize that SLs function as modulators used by plants to switch between two growth forms: a bushier form displaying a strong outgrowth of many side shoots and a weak main stem, and a form in which the main shoot dominates and displays enhanced secondary growth. The ability to oscillate to a certain extent between these growth forms could be regarded as being beneficial if, for example, differences in the necessity to compete for light, or in the total number of flowers produced by the shoot system under changing environmental conditions, are considered. This feature could represent a strategy in which the plant can choose the optimal way to grow to cope with the challenges imposed by a sessile lifestyle.

Materials and Methods

Details about growth conditions, cloning and plant lines, histological analyses, pharmacological treatments, RT-PCR, auxin measurements, and other techniques are in SI Materials and Methods. Arabidopsis thaliana (L.) Heynh. plants of the accession Columbia were used with the exception of the PXY:GUS reporter line, which is in the Ler background (38).

Acknowledgments

We are grateful to Ottoline Leyser for providing the max1-1, max2-1, max3-9, max4-1, axr1-3 max1-1, and axr1-3 max2-1 mutant lines; Christian Luschnig for providing the pin3-5 mutant; and Simon Turner for providing the PXY:GUS marker line. This work was supported by Austrian Science Fund (FWF) Grants P21258-B03 and P23781-B16 (to M.S., P.S., and J.A.) the Wiener Wissenschafts-, Forschungs-, und Technologiefonds (T.S.), the Australian Research Council (E.A.D., P.B.B., and C.A.B.), and the Swedish Governmental Agency for Innovation Systems and the Swedish Research Council (K.L.).

(2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol155:974–987.

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